Sensory Stimulation Influences Neuronal Growth

The potential involvement of afferent innervation in regulating dendrite growth originates from a rich history of studies in which animals are reared under conditions of altered sensory stimulation. Animals raised in environments enriched with complex sensory stimuli and mentally challenging activities develop cortical neurons with more complex dendritic arbors compared to neurons of animals reared in less stimulating environments37-39. More drastic interventions created by sensory occlusion demonstrate that loss of normal activity during development leads to lasting alterations in dendritic morphology. Dark rearing during critical periods of visual system development alters the pattern and distribution of dendrites of layer 4 dendrites in rat visual cortex40. Monocular deprivation alters dendrite development in lateral geniculate nucleus (LGN) and visual cortex41,42, with dendrites of denervated layer 4 cortical spiny stellate neurons abnormally extending into neighboring nondeprived ocular dominance columns43. Further evidence of afferent input directing dendrite growth comes from the three-eyed frog in which the additional retinal input creates abnormal ocular dominance bands in the tectum, and dendritic arbors of tectal neurons are restricted to regions innervated by one eye44. Afferent input-regulated growth is not limited to the visual system since occluding auditory input by plugging one ear results in shortening of dendrites of laminar nucleus neurons innervated by that ear45. However, visual deprivation does not significantly alter dendritic growth of cortical layer 4 stellate cells46 or layer 3 pyramidal cells47, suggesting that factors besides neuronal activity associated with external sensory stimulation may promote correct arborization. Findings that de-afferentation produces a profound reduction in dendrite length, exceeding effects of occluding sensory input, imply that spontaneous activity or activity-independent mechanisms substantially contributes to growth48. The coexistence of multiple mediators of growth in addition to correlated afferent input, including spontaneous activity and activity-independent mechanisms that remain following sensory occlusion likely contributes to these varying results.

Important direct evidence for sensory stimuli regulating growth of brain neurons was shown using in vivo repeated time-lapse imaging of developing Xenopus tectal neurons15. Sin and colleagues took advantage of the ability to transfect newly formed neurons in the tectal proliferative zone and the subsequent growth of these neurons into a functional visual processing circuit. The primary afferent input to tectal neurons at this stage is glutamatergic synaptic input from retinal ganglion cells (RGCs), and tectal neurons respond to visual stimuli. Sin and colleagues controlled afferent glutamatergic innervation to tectal neurons by altering visual stimulation for short periods while directly imaging effects on growth of developing tectal neuron dendrites using in vivo two-photon microscopy. They find that exposure to brief periods (4 h) of darkness or visual stimulation induced decreased and increased growth, respectively. The increased dendrite growth during visual stimuli was mediated by an increase in new branch additions and filopodial stabilization. Further experiments found that when a brief period of visual stimulation precedes exposure to darkness, the growth-promoting effects of patterned visual stimulation persists even after the stimulus is removed. This suggests that sensory stimulation triggers long-lasting increased morphological plasticity that becomes independent of persistent activity.

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